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Human PSC-derived organoids model sympathetic ganglion development and its functional crosstalk with the heart

ABSTRACT: The sympathetic ganglia are essential components of the nervous system that regulate various aspects of involuntary body functions. Recapitulating sympathetic ganglion development with three-dimensional (3D) organoids is challenging and has not been achieved. Here, we report a method to differentiate human pluripotent stem cells into 3D neural organoids that resemble peripheral sympathetic ganglia, producing both neurons and glial cells of the ganglia in a self-organized manner. We developed an organoid system to construct functional connections between the sympathetic ganglia and one of their peripheral targets, the heart, by fusing human sympathetic ganglion organoids (hSGOs) and heart-forming organoids. Notably, this system enables the evaluation of signaling controls (i.e., nerve growth factor [NGF] signaling) on human sympathetic-to-cardiac innervation and reveals the reciprocal impacts between the sympathetic and cardiac lineages during their co-development. Our study provides a physiologically relevant platform for understanding the development of human sympathetic ganglia, their crosstalk with peripheral targets, and related diseases.

ORGANISM(S): Homo sapiens

PROVIDER: GSE294956 | GEO | 2025/12/11

REPOSITORIES: GEO

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Project description:The cardiac autonomic nervous system is crucial in controlling cardiac function, such as heart rate and cardiac contractility, and is divided into sympathetic and parasympathetic branches. Normally, there is a balance between these two branches to maintain homeostasis. However, cardiac disease states such as myocardial infarction, heart failure, and hypertension can induce the remodeling of cells involved in cardiac innervation, which is associated with an adverse clinical outcome. Although there are vast amounts of data for the histological structure and function of the cardiac autonomic nervous system, its molecular biological architecture in health and disease is still enigmatic in many aspects. Novel technologies such as single-cell RNA sequencing (scRNA-seq) hold promise for the genetic characterization of tissues at single-cell resolution. However, the relatively large size of neurons may impede the standardized use of these techniques. Here, this protocol exploits droplet-based single-nucleus RNA sequencing (snRNA-seq), a method to characterize the biological architecture of cardiac sympathetic neurons in health and disease. A stepwise approach is demonstrated to perform snRNA-seq of the bilateral superior cervical (SCG) and stellate ganglia (StG) dissected from adult mice. This method enables long-term sample preservation, maintaining an adequate RNA quality when samples from multiple individuals/experiments cannot be collected all at once within a short period of time. Barcoding the nuclei with hashtag oligos (HTOs) enables demultiplexing and the trace-back of distinct ganglionic samples post sequencing. Subsequent analyses revealed successful nuclei capture of neuronal, satellite glial, and endothelial cells of the sympathetic ganglia, as validated by snRNA-seq. In summary, this protocol provides a stepwise approach for snRNA-seq of sympathetic extrinsic cardiac ganglia, a method that has the potential for broader application in studies of the innervation of other organs and tissues.

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Human PSC-derived organoids model sympathetic ganglion development and its functional crosstalk with the heart

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